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Of dups and dinos: evolution at the K/Pg boundary
Rolf Lohaus1,2,3 and Yves Van de Peer1,2,3,4
Fifteen years into sequencing entire plant genomes, more than
30 paleopolyploidy events could be mapped on the tree of
flowering plants (and many more when also transcriptome data
sets are considered). While some genome duplications are very
old and have occurred early in the evolution of dicots and
monocots, or even before, others are more recent and seem to
have occurred independently in many different plant lineages.
Strikingly, a majority of these duplications date somewhere
between 55 and 75 million years ago (mya), and thus likely
correlate with the K/Pg boundary. If true, this would suggest
that plants that had their genome duplicated at that time, had
an increased chance to survive the most recent mass extinction
event, at 66 mya, which wiped out a majority of plant and
animal life, including all non-avian dinosaurs. Here, we review
several processes, both neutral and adaptive, that might
explain the establishment of polyploid plants, following the
K/Pg mass extinction.
Brassicaceae species may be neopolyploids [2]. The apparent paucity of ancient genome duplications and the
existence of so many species that are currently polyploid
provide an interesting and fascinating enigma. Part of this
observation can probably be explained by the fact that
because evolutionary relationships form a tree, with most
ancient lineages extinct, there are simply fewer places on
the ‘older’ parts of the tree to observe a polyploidy event
than on the tips of the tree. It is possible that we
see relatively few ancient WGDs because only a few of
the lineages that existed at those times have survived to
the present for us to observe them. Nevertheless, it
remains true that even for plant lineages that have not
gone extinct and have existed for a long time, the total
number of established ancient WGDs is usually very
limited.
Addresses
1
Department of Plant Biotechnology and Bioinformatics, Ghent
University, Ghent, Belgium
2
Department of Plant Systems Biology, VIB, Ghent, Belgium
3
Bioinformatics Institute Ghent, Ghent University, Ghent, Belgium
4
Genomics Research Institute, University of Pretoria, Pretoria, South
Africa
Thus, although the prevalence of WGDs has been firmly
established, their attributed importance remains controversial [3]. Despite being considered by many as an
evolutionary dead end [4,5], at some time in evolution,
organisms that have undergone WGDs have unequivocally had an adaptive advantage, because so many descendants share the same duplication event. Well-known
examples are for instance ancient genome duplications at
the base of the flowering tree [6], but also at the base of
the dicots [7], the monocots [8,9], and on branches leading
to important plant families [10,11,12,13].
Corresponding author: Van de Peer, Yves
([email protected])
Current Opinion in Plant Biology 2016, 30:62–69
This review comes from a themed issue on Genome studies and
molecular genetics
Edited by Yves Van de Peer and J Chris Pires
http://dx.doi.org/10.1016/j.pbi.2016.01.006
1369-5266/# 2016 The Authors. Published by Elsevier Ltd. This is an
open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Analysis of whole genome sequences shows that the longterm establishment of ancient organisms that have
undergone whole genome duplications (WGDs, paleopolyploids) has been rare, even for flowering plants, where
the majority of ancient WGDs have been observed [1].
Indeed, during the last 150–200 million years of plant
evolution, some lineages have experienced maybe four to
five WGDs, but most no more than one or two (Figure 1).
On the other hand, tens of thousands of now-living
species, both plants and animals, are polyploid, and
contain multiple copies of their genome. For example,
it has recently been estimated that 43% of the 3700
Current Opinion in Plant Biology 2016, 30:62–69
A question that has received much attention of late is
whether these older genome duplications have survived
by coincidence or because they did occur, or were selected for, at very specific times, for instance during times of
major ecological or environmental upheaval, and/or periods of extinction [3]. Indeed, it has been proposed that
chromosome doubling conveys greater stress tolerance by
for instance fostering slower development, delayed reproduction, longer life span, and greater defense against
pathogens and herbivores. Furthermore, polyploids have
also been considered to have greater ability to colonize
new or disturbed habitats [14]. There is thus growing
evidence that WGDs might be correlated with so-called
major events in evolution. One of the most striking cases
is a wave of WGDs in flowering plants at the Cretaceous–
Paleogene (K/Pg) boundary [3,11,15], as outlined in
Figure 1. This boundary is marked by a bolide impact
near Chicxulub (Mexico) and a possibly impact-induced
increase in Deccan flood volcanism (India) [16], which
caused, among others, the extinction of all non-avian
dinosaurs and massive disruption of plant communities
with an estimated extinction of 30–60% of plant species
and global deforestation [17,18]. Many of the WGDs
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Genome evolution at the K/Pg boundary Lohaus and Van de Peer 63
Figure 1
Jurassic
Cretaceous
Tertiary
Eurosids I
Cucumis melo
Cucumis sativus
Citrullus lanatus
Juglans regia
Malus domestica
Pyrus bretschneideri
Prunus persica
Prunus mume
Fragaria vesca
Glycine max
Cajanus cajan
Medicago truncatula
Cicer arietinum
Lotus japonicus
Ricinus communis
Manihot esculenta
Jatropha curcas
Linum usitatissimum
Populus trichocarpa
Salix suchowensis
Brassica rapa
Thelungiella parvula
Arabidopsis thaliana
Arabidopsis Iyrata
Carica papaya
Theobroma cacao
Gossypium raimonddi
Eucalyptus grandis
Vitis vinifera
Solanum Iycopersicum
Solanum tubersomum
Sesamum indicum
Lactuca sativa
Nelumbo nucifera
Aquilegia formosa x pubescens
Brachypodium distachyon
Hordeum vulgare
Oryza sativa
Zea mays
Sorghum bicolor
Setaria italica
Ananas comosus
Musa acuminata
Phoenix dactylifera
Phalaenopsis equestris
Spirodela polyrhiza
Zostera marina
Nuphar advena
Equisetum giganteum Horsetails
Moss
Physcomitrella patens
Eudicots
Eurosids II
Asterids
150
125
100
75
50
25
Monocots
175
Mya
Current Opinion in Plant Biology
Schematic tree showing the evolutionary relationship between plants for which the genome sequence has been published. WGDs described in
previous studies [9,11,12,13,84–86] are mapped onto the tree (red and pink rectangles). WGDs estimated between 55 and 75 million years old
(shaded area around the K/Pg boundary, red line) are indicated by pink rectangles. See text for details.
clustered around the K/Pg extinction event are at the base
of some of the largest and most successful extant plant
families suggesting that polyploidy appears to be correlated with plant survival through the K/Pg boundary [3].
Another example of WGDs that might be correlated with
decisive moments in plant evolution has recently been
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described by Estep et al. [19]. These authors showed a
wave of allopolyploidizations in C4 grasses coincident
with the worldwide expansion of C4 grasslands. Grasses
using C4 photosynthesis rose to ecological dominance and
displaced C3 grasslands starting in the Late Miocene,
after an earlier decrease of atmospheric CO2 levels in the
Oligocene and a forest-to-C3-grassland transition in the
Current Opinion in Plant Biology 2016, 30:62–69
64 Genome studies and molecular genetics
Early-Middle Miocene [20]. In the ecologically dominant
and economically important grass tribe Andropogoneae
(which includes maize (Zea mays), sorghum, and sugarcane (Saccharum officinarum)), the authors found at least
32% of the 1200 species to be allopolyploids. More
remarkably, these are the result of a minimum of 34 distinct polyploidy events, most of which occurred during
the expansion of the C4 grasslands. Polyploidy hence also
seems to be correlated with dominance of C4 over C3
grasses and large-scale displacement of the latter [19].
Other evidence for a major role of polyploidy (alone or in
conjunction with hybridization) in plant invasion success
has been accumulating in recent years [14,21–23]. For
instance, Pandit et al. [24] compared ploidy levels among
rare and invasive plant species on a worldwide scale, and
found that polyploids are 20% more likely to be invasive
than closely related diploids.
Clearly, the correlations of polyploidization with both
plant survival at the K/Pg boundary and plant invasiveness in general are related, as the plant survivors of the
K/Pg mass extinction event turned into plant invaders and
recolonizers of the post-cataclysmic, low-plant diversity
environment. The signature of the WGDs that got established around the K/Pg boundary could thus stem from
these polyploidization events being linked to plant survival, being linked to plant invasiveness post-survival, or
both. In each case, the particular WGDs could have been
adaptive, that is, enhancing survival and/or invasiveness,
while also more neutral processes could have led to an
increase in the production or occurrence of plant polyploids [11]. Examples of the latter could be environmental stress causing an increase in unreduced gamete
formation [25], or contact/overlap between divergent
expanding populations or species causing an increase in
hybridization and allopolyploid formation. Likely, it has
been a (potentially species-specific and environmentspecific) mixture of all of the above.
In the following, we elaborate on several processes,
neutral and adaptive, that associate WGD with plant
survival and/or invasiveness, and which could individually
or in combination be responsible for the observed pattern
of plant (genome) evolution at the K/Pg boundary. We
review some of the supporting evidence and particularly
highlight some recent studies that investigate the adaptive role of polyploids in this context using experimental
or modeling approaches.
Survival and extinction in devastated plant
populations (aka out-surviving dinosaurs)
Polyploidy undoubtedly can have detrimental effects on
phenotype, and these have long been recognized [4,26].
For instance, genomic instability, mitotic and meiotic
abnormalities, and gene expression and epigenetic
changes following polyploidization [27–29] — often collectively termed ‘genomic shock’ — can lead to increased
Current Opinion in Plant Biology 2016, 30:62–69
sterility and decreased fitness, at least for polyploids
within stable populations of well-adapted diploid progenitors. Nevertheless, stable polyploids can commonly
be found in many natural plant populations because
polyploidization occurs at relatively high frequency in
plants, and some polyploid lineages do stabilize and avoid
immediate extinction [30–34].
During the environmental and ecological upheaval at the
K/Pg boundary, existing or naturally occurring polyploids
could have had higher survival or lower extinction rates
than the existing diploids [3,35]. The massive loss of plant
life likely resulted in more fragmented, isolated and small
populations, which could suffer from the negative effects
of genetic bottlenecks such as increased drift and inbreeding. Polyploidy could have provided several benefits in such populations. An immediate advantage of a
newly formed polyploid is the creation of redundant
genes, which has the effect that deleterious recessive
alleles can be masked [21,36]. This could, at least temporarily, reduce inbreeding depression [37,38]. Gene
redundancy could also increase robustness (the buffering
of genetic or environmental perturbations), at the gene
and/or network level [38–40]. Increased genetic robustness could result in lower genetic load in polyploids
compared to diploids, but could also potentially be opposed by the larger mutational target size and by dosage
balance constraints once deleterious mutations accumulate [41,42]. That polyploids could have higher fitness in
harsh conditions and increased stress tolerance (environmental robustness) has been proposed repeatedly and is
supported by a number of studies (reviewed in [14], see
also [43]), as well as by the observation that present-day
polyploids, particularly younger ones, tend to occur more
in disturbed environments [44,45]. To which extent
environmental robustness is promoted by gene duplicates and/or redundancy or is the result of other mechanisms is, however, unclear. Another characteristic of
small populations is that the strength of selection is
reduced and thus some deleterious mutations may effectively be neutral. This could result in a smaller disadvantage of polyploids with decreased fitness compared to
their diploid progenitors.
Polyploidy is often accompanied with a switch to selfing
or apomixis (asexual reproduction) [46,47]. This may
increase the chances of polyploids to survive or help avoid
extinction for the following reasons. In small populations,
strong selection for the most efficient reproductive mode
may operate [48,49]; polyploids could be able to respond
to such selection, or be selected for if variation in reproductive strategy preexists in the population. Asexual or
selfing polyploids may have an advantage if suitable
mating partners are scarce, and they would overcome
the minority cytotype disadvantage inherent to polyploids [50]. A shift to asexuality or self-fertilization also
releases a polyploid from recombination load which could
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Genome evolution at the K/Pg boundary Lohaus and Van de Peer 65
temporarily further reduce its genetic load compared to
its diploid sexual progenitors [51], and this in addition to
its potential gain in mutational robustness mentioned
above.
Existing allopolyploids can exhibit heterosis, or hybrid
vigor [29], and fixed heterozygosity, resulting in a strong
competitive advantage over diploid progenitors [26], particularly in bottlenecked populations. Several other potential advantages of polyploids over diploids related to
enhanced survival in harsh or new conditions have been
described, particularly with regard to plant invasiveness
(e.g., reviewed in [14]). Among them are morphological
changes leading to, for example, higher seed mass and
seedling vigor; niche differentiation, where polyploids
favor drier and more open habitats; changes in biotic
interactions which may result in, for example, higher
pathogen resistance [52,53] or lower insect herbivory in
polyploids [54]. There are several examples from the
literature on plant invasions that show pre-adaptation
of existing polyploids to become invasive, for example,
by allowing them to avoid or mitigate founder effects
when established in the invasive range, or by possessing
simply by chance a divergent phenotype that is close to
the optimum under the new environmental conditions
[1,14,23,32]. The underlying mechanisms or processes
are the same or similar to the ones outlined above, thus
they may be applicable to also facilitate pre-adaptation of
existing polyploids to survive in small populations in a
drastically changed environment.
(Neutral) drivers of increased plant
polyploidization (aka out-duplicating
dinosaurs)
Apart from the potential survival benefits that existing or
naturally occurring polyploids might have had at the K/Pg
boundary, more neutral processes could have contributed
to the observed establishment of polyploids by passively
or actively increasing the frequency with which polyploids were created. We will briefly review two of these.
Unreduced gamete production is most probably the major
mechanism of polyploid formation in plants [30], and it
has recently been suggested that it may constitute an
evolutionary mechanism for plant speciation and/or
stress-response [11,55]. A substantial number of studies have documented that environmental stress and/or
fluctuations (particularly, heat and cold stress and fluctuating temperatures, but also stresses such as herbivory or
disease) trigger increased formation of unreduced
gametes [25,30,56,57]. Additional support for this link
comes from the discoveries of increased numbers of
unreduced fossil gametes from the time of the End
Triassic (fossil pollen from an extinct conifer group
[58]) and End Permian extinction events (fossil gymnosperm pollen and lycophyte spores [59,60]). Importantly,
unreduced gamete production is a highly heritable trait
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and genetic variation for the ability to produce unreduced
gametes exists for selection to act on [61,62]. These and
other [11,55] lines of evidence all point to unreduced
gamete formation and hence polyploidization as a potential evolutionary survival mechanism in response to environmental and/or ecological disaster. Oswald and
Nuismer [32] developed a mathematical model in which
polyploids with no intrinsic fitness benefits arise in a
diploid population at low frequency. Their results showed
that in a rapidly changing but not in a constant environment a higher rate of unreduced gamete formation increased the probability of polyploids to replace their
diploid progenitors. Alternatively, or in addition to being
increased mechanistically, the relative frequency of unreduced gametes could have also been increased more
neutrally at the K/Pg boundary by the more dominant
role of genetic drift under small population sizes. In small
post-cataclysm plant communities this could have led to
(even) higher numbers of unreduced gametes by random
chance events, thereby increasing the probability of matings leading to polyploidy [63].
Another, related process that could have resulted in
neutrally increased levels of polyploids is intensified
hybridization around the time of the K/Pg boundary.
The (re)expansion of decimated and fragmented plant
populations and (re)colonization of desolated or deforested habitats is likely to have caused both intraspecific
and interspecific hybrid formation within new contact
zones. Hybridization can lead to (see below) or is at least
closely associated with polyploidization, as the latter
stabilizes hybrids affected by genomic shock [64], and
prevents hybrid sterility or restores sexual reproduction
[21]. Consistently, hybridization is common in regions
currently affected by plant invasions (e.g., [65,66]), and a
recent meta-analysis showed a high percentage of polyploids among invasive and weedy plant hybrids [22].
There is some evidence that suggests that the high rate
of allopolyploidizations in C4 grasses, mentioned earlier,
is driven by the expansion of the grasslands which led to
hybridizations between divergent diploid progenitor species [19]. Furthermore, interspecific hybrids themselves
have markedly increased levels of unreduced gamete
production, thus facilitating allopolyploidization [30],
and unreduced gametes are themselves also being involved in hybridization events [55].
Enhanced evolvability of polyploid plant
survivors (aka adaptive blooming in a
dinosaur-free world)
Whichever of the processes outlined in the previous two
sections generated new, or maintained or increased existing levels of plant polyploids, these polyploids could
possess or have an increased capacity to gain adaptive
advantages in their stressed, changing or new environment,
enabling selection to reinforce or drive polyploid establishment. Such higher adaptive potential of polyploids has long
Current Opinion in Plant Biology 2016, 30:62–69
66 Genome studies and molecular genetics
been recognized and discussed [10,14,26,45,67]. Most
explanations center around the creation of genetic variation by WGDs leading to increased phenotypic variability
and/or plasticity [68–71], or even to novel phenotypes, for
example, more extreme, transgressive ones [72,73]. Under
new and challenging conditions, this variation then provides ‘fuel’ for evolution and could thus result in polyploids
having a higher capacity for adaptation than their diploid
progenitors. Consequently, polyploidy has been associated
with the tolerance of a broader range of ecological and
environmental conditions, and increased invasion and colonization success, with some evidence supporting each of
these ([24,70]; examples in te Beest et al. [14]). Such
attributes could certainly have been advantageous for
exploiting a devastated global ecosystem, potentially
explaining the clustering of WGDs at the K/Pg boundary,
as suggested before [11,15]. Similarly, the recurrent
allopolyploidizations in C4 grasses could have allowed
range expansions and thus driven formation of global C4
grasslands, one of the most remarkable examples of biome
evolution; this is an alternative hypothesis to the opposite,
grassland expansions driving polyploidization, as described
in the previous section [19,20].
Two sources of increased genetic variation in polyploids
are most commonly recognized: genomic shock (see
above) and introgression. Polyploids could also harbor
higher levels of pre-existing cryptic or standing genetic
variation. WGDs create genetic redundancy, which could
lead to an increase in genetic robustness. Both enlarge
neutral genotype space and allow for the buildup of
cryptic genetic variation [74–77]. Adaptation from such
pre-existing genetic variation can be fast (compared to
adaptation from new beneficial mutations); for instance, it
has recently been shown that selection on standing genetic variation drove early adaptation in flowering time in
a colonizing population of (the non-polyploid) Pyrenean
Rocket [78].
of wild tetraploid Achillea borealis in the hexaploid dune
habitat [80]. The results suggest that both WGD per se as
well as post-WGD evolution conferred adaptation to the
novel dune habitat. Cuypers and Hogeweg [81,82] developed a computational model of simple metabolic
dynamics in a virtual unicellular organism and used
population-based simulations to study evolutionary and
genomic consequences of WGDs. A major aim was to
investigate if WGDs could increase the ability of model
organisms to adapt to a wide range of new environments.
They found that establishment of WGDs was very common in the initial standard environment before the
change, but that only a minority of populations established subsequent WGDs during adaptation to one of the
new environments after the environmental change, with
establishment of WGDs being particularly rare in rapidly
re-adapting populations [82]. Nevertheless, the authors
claim that WGDs did improve the ability of populations
to adapt to a changed environment. However, 80% of the
majority of populations that did not establish WGDs
during re-adaptation were equally able to adapt to a
changed environment, and often more rapidly. Due to
these incongruities and because we believe the experimental design and analysis was inadequate to test the
above hypothesis, we feel that the results and conclusions
of this study should be treated with caution. For example,
in their simulation protocol neither the occurrence, nor
the number, nor the timing of WGDs before the environmental change was a controlled independent variable, but
any of these could have had an effect on the ability to
adapt to the environmental change. More importantly, we
also suspect that those few post-change WGDs that did
establish in populations and led to a higher adaptability
did so almost exclusively only in a specific subset of new
environments whose characteristics — high enzyme degradation rates — gave organisms with WGDs a ‘built-in’
advantage.
Conclusions
Direct tests of the hypothesis that WGDs can enhance or
accelerate evolutionary adaptation to new or changing
environments are difficult to conduct and therefore rare.
Selmecki et al. [79] recently used an experimental
evolution approach to test the effect of yeast ploidy on
the speed of adaptation to a nutrient-limited environment. They found that tetraploid yeast showed significantly faster adaptation than diploid or haploid yeast, and
that tetraploidy increased the amount of genetic variation
within a population. Using mathematical modeling they
attributed the higher rate of adaptation in polyploids to
increased frequency and fitness effects of beneficial
mutations in these populations, and whole-genome sequencing supported post-WGD genomic instability as
one of the sources of these mutations. Another elegant
experimental study used field transplant experiments to
compare fitness of both wild hexaploid and artificial
neohexaploid wild yarrow (Achillea borealis) against fitness
Current Opinion in Plant Biology 2016, 30:62–69
Since the origin of the flowering plants, whole genome
duplication events have been identified in many different plant lineages. Strikingly however, in many lineages,
which are often over a hundred million years old (see
Figure 1), we have evidence for only one (sometimes
two, rarely three) WGD event(s) that got established in
the long term, although many more WGDs must have
occurred during the evolutionary past of these lineages.
Even more strikingly, in a majority of cases, this
WGD event seems to have occurred close to the K/Pg
boundary, shaped by the most recent mass extinction
event, about 66 mya, which wiped out a major part of
plant and animal life, including all non-avian dinosaurs.
Apparently, many plants we are so familiar with (or
better their ancestors) had or gained a duplicated genome at that time, which gave them a selective advantage compared to their diploid progenitors, who went
extinct.
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Genome evolution at the K/Pg boundary Lohaus and Van de Peer 67
When we first speculated on the tentative link between
some of the known paleopolyploidization events in
plants and the K/Pg boundary, and suggested that
WGD was linked to plant survival around that time
[15], this was met with skepticism because of the limited
amount of data available at that time, and because
dating ancient events that occurred tens of millions of
years ago is not trivial. Therefore, we recently revisited
this hypothesis using many more whole genome
sequences and more sophisticated models of molecular
evolution and tree dating, and concluded that our initial
findings were confirmed [11]. We have also considered
the possibility whether dating a majority of WGDs
between 55 and 75 mya might be due to technical or
methodological issues, rather than reflecting true dates
of duplication. Although we could show, with statistical
support, that the inferred dates for many of the WGDs
are clustered in time [11,15], a correlation between
WGDs and the K/Pg extinction would not hold much
significance if WGD events in this time window are
simply easier to detect than older or younger WGDs,
because, for instance, more ancient events are obscured
by more recent events, or because more recent events
may be hard to distinguish from other genomic duplication processes. However, we do not believe this to be
the case. First, both younger and older WGDs have been
reported (see Figure 1) based on KS age distributions
from synonymous substitutions and phylogenomic
approaches, two inherently different methods that generally do not suffer from the same methodological issues
[3,83]. Second, we do have the bioinformatics tools (e.g.,
for detecting within-genome colinearity) to see, in most
cases, whether multiple rounds of whole genome duplications have occurred and/or how duplicates were generated.
Here, we discussed three, not mutually exclusive, groups
of processes that could explain this clustering of WGDs
around the K/Pg boundary: (1) existing and/or naturally
occurring polyploids had higher survival or lower extinction rates, (2) the rate of polyploid formation increased
and hence the relative frequency of polyploids and their
chance of fixation, and (3) polyploid survivors of the
cataclysm had higher post-cataclysm adaptive and/or invasive potential. Thus, both adaptive and more neutral
processes likely contributed to promote the establishment of polyploid plants at a time when a catastrophic
event of global scale led to a much more challenging and
transformed environment.
Acknowledgements
The authors acknowledge the Multidisciplinary Research Partnership
‘Bioinformatics: from nucleotides to networks’ Project (no. 01MR0310W) of
Ghent University and the European Union Seventh Framework Programme
(FP7/2007-2013) under European Research Council Advanced Grant
Agreement 322739-DOUBLEUP. We apologize to those whose work could
not be cited because of space limitations. We also thank two reviewers for
their constructive and insightful comments.
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